Differences in fat and muscle mass associated with a functional human polymorphism in a post-transcriptional BMP2 gene regulatory element

Journal of Cellular Biochemistry

Volumn 107, Issue 6, 2009, Pages 1073-1082

  Devaney, Joseph M ^a   Tosi, Laura L ^b   Fritz, David T ^c   Gordish Dressman, Heather A ^a   Jiang, Shan ^c,m   Orkunoglu Suer, Funda E ^a   Gordon, Andrew H ^d   Harmon, Brennan T ^a   Thompson, Paul D ^e   Clarkson, Priscilla M ^f   Angelopoulos, Theodore J ^g   Gordon, Paul M ^h   Moyna, Niall M ⁱ   Pescatello, Linda S ^j   Visich, Paul S ^k   Zoeller, Robert F ^l   Brandoli, Cinzia ^a   Hoffman, Eric P ^a   Rogers, Melissa B ^c  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^d GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^e HARTFORD HOSPITAL   (United States)

^f UNIVERSITY OF MASSACHUSETTS   (United States)

^g UNIVERSITY OF CENTRAL FLORIDA   (United States)

^h UNIVERSITY OF MICHIGAN   (United States)

ⁱ DUBLIN CITY UNIVERSITY   (Ireland)

^j UNIVERSITY OF CONNECTICUT   (United States)

^k CENTRAL MICHIGAN UNIVERSITY   (United States)

^l FLORIDA ATLANTIC UNIVERSITY   (United States)

^m Gene Tools LLC   (United States)

more..

Author keywords

Bone Morphogenetic Protein 2 (BMP2); Fitness; Mesenchymal cells; Messenger RNA (mRNA); Population genetics; Post transcriptional gene regulation; Single Nucleotide Polymorphism (SNP)

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; LUCIFERASE;

ADULT; AMINO ACID SEQUENCE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME SYNTHESIS; FEMALE; GENE FREQUENCY; GENETIC VARIABILITY; HUMAN; IN VITRO STUDY; MALE; MESENCHYME CELL; MUSCLE MASS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA BINDING; SINGLE NUCLEOTIDE POLYMORPHISM; SUBCUTANEOUS FAT;

ADIPOSE TISSUE; ADOLESCENT; ADULT; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CELL LINE; FEMALE; GENOTYPE; HUMANS; MALE; MICE; MUSCLE, SKELETAL; PHYSICAL FITNESS; POLYMORPHISM, SINGLE NUCLEOTIDE; REGULATORY SEQUENCES, NUCLEIC ACID; RESISTANCE TRAINING; YOUNG ADULT;

MAMMALIA; PISCES;

EID: 68049113350     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22209     Document Type: Article

References (53)

1. Abrams KL, Xu J, Nativelle-Serpentini C, Dabirshahsahebi S, Rogers MB. 2004. An evolutionary and molecular analysis of Bmp2 expression. J Biol Chem 279:15916-15928. (Pubitemid 38509279)
2. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 1997. Current protocols in molecular biology. NY: Wiley and Sons.
3. Balint E, Lapointe D, Drissi H, van der Meijden C, Young DW, van Wijnen AJ, Stein JL, Stein GS, Lian JB. 2003. Phenotype discovery by gene expression profiling: Mapping of biological processes linked to BMP-2-mediated osteoblast differentiation. J Cell Biochem 89:401-426. (Pubitemid 36547274)
4. Cheng SL, Shao JS, Charlton-Kachigian N, Loewy AP, Towler DA. 2003. MSX2 promotes osteogenesis and suppresses adipogenic differentiation of multipotent mesenchymal progenitors. J Biol Chem 278:45969-45977. (Pubitemid 37432744)
5. Conne B, Stutz A, Vassalli JD. 2000. The 3′ untranslated region of messenger RNA: A molecular 'hotspot' for pathology? Nat Med 6:637-641.
6. Denker AE, Haas AR, Nicoll SB, Tuan RS. 1999. Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: I. Stimulation by bone morphogenetic protein-2 in high-density micromass cultures. Differentiation 64:67-76.
7. Dreyfuss G, Kim VN, Kataoka N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3:195-205. (Pubitemid 37237142)
8. Feng JQ, Chen D, Ghosh-Choudhury N, Esparza J, Mundy GR, Harris SE. 1997. Bone morphogenetic protein 2 transcripts in rapidly developing deer antler tissue contain an extended 5′ non-coding region arising from a distal promoter. Biochim Biophys Acta 1350:47-52. (Pubitemid 27025930)
9. Feng JQ, Xing L, Zhang JH, Zhao M, Horn D, Chan J, Boyce BF, Harris SE, Mundy GR, Chen D. 2003. NF-kappaB specifically activates BMP-2 gene expression in growth plate chondrocytes in vivo and in a chondrocyte cell line in vitro. J Biol Chem 278:29130-29135. (Pubitemid 36935828)
10. Fritz DT, Ford LP, Wilusz J. 2000. An in vitro assay to study regulated mRNA stability. Sci STKE 2000:PL1.
11. Fritz DT, Jiang S, Xu J, Rogers MB. 2006. A polymorphism in a conserved posttranscriptional regulatory motif alters bone morphogenetic protein 2 (BMP2) RNA:protein interactions. Mol Endocrinol 20:1574-1586. (Pubitemid 43967565)
12. Fritz DT, Liu D, Xu J, Jiang S, Rogers MB. 2004. Conservation of Bmp2 post-transcriptional regulatory mechanisms. J Biol Chem 279:48950-48958. (Pubitemid 39625776)
13. Fukui N, Ikeda Y, Ohnuki T, Hikita A, Tanaka S, Yamane S, Suzuki R, Sandell LJ, Ochi T. 2006. Pro-inflammatory cytokine tumor necrosis factor-alpha induces bone morphogenetic protein-2 in chondrocytes via mRNA stabilization and transcriptional up-regulation. J Biol Chem 281:27229-27241. (Pubitemid 44401752)
14. Ghosh-Choudhury N, Choudhury GG, Harris MA, Wozney J, Mundy GR, Abboud SL, Harris SE. 2001. Autoregulation of mouse BMP-2 gene transcription is directed by the proximal promoter element. Biochem Biophys Res Commun 286:101-108. (Pubitemid 32917655)
15. Heller LC, Li Y, Abrams KA, Rogers MB. 1999. Transcriptional regulation of the Bmp2 gene: Retinoic acid induction in F9 embryonal carcinoma cells and Saccharomyces cerevisiae. J Biol Chem 274:1394-1400. (Pubitemid 129507726)
16. Hogan B. 1996. Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev 10:1580-1594. (Pubitemid 26268864)
17. Jiang S, Zhang S, Langenfeld J, Lo SC, Rogers MB. 2007. Mycoplasma infection transforms normal lung cells and induces bone morphogenetic protein 2 expression by post-transcriptional mechanisms. J Cell Biochem 104:580-594. (Pubitemid 351671646)
18. Kang Q, Song WX, Luo Q, Tang N, Luo J, Luo X, Chen J, Bi Y, He BC, Park JK, Jiang W, Tang Y, Huang J, Su Y, Zhu GH, He Y, Yin H, Hu Z, Wang Y, Chen L, Zuo GW, Pan X, Shen J, Vokes T, Reid RR, Haydon RC, Luu HH, He TC. 2009. A comprehensive analysis of the dual roles of BMPs in regulating adipogenic and osteogenic differentiation of mesenchymal progenitor cells. Stem Cells Dev 18:1-18.
19. Karasik D, Kiel DP. 2008. Genetics of the musculoskeletal system: A pleiotropic approach. J Bone Miner Res 23:788-802. (Pubitemid 351768797)
20. Katagiri T, Yamaguchi A, Ikeda T, Yoshiki S, Wozney JM, Rosen V, Wang EA, Tanaka H, Omura S, Suda T. 1990. The non-osteogenic mouse pluripotent cell line, C3H10T1/2, is induced to differentiate into osteoblastic cells by recombinant human bone morphogenetic protein-2. Biochem Biophys Res Commun 172:295-299. (Pubitemid 20352535)
21. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T, Rosen V, Wozney JM, Fujisawa-Sehara A, Suda T. 1994. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 127:1755-1766. (Pubitemid 24380911)
22. Li Z, Hassan MQ, Volinia S, van Wijnen AJ, Stein JL, Croce CM, Lian JB, Stein GS. 2008. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci USA 105:13906-13911.
23. Liu D, Fritz DT, Rogers MB, Shatkin AJ. 2008. Species-specific cis-regulatory elements in the 3′UTR direct alternative polyadenylation of bone morphogenetic protein 2 mRNA. J Biol Chem 283:28010-28019.
24. Manolagas SC, Almeida M. 2007. Gone with the Wnts: Beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol 21:2605-2614. (Pubitemid 350035144)
25. McGuigan F, Larzenius E, Callreus M, Gerdhem P, Luthman H, Akesson K. 2008. Variation in the bone morphogenetic protein-2 gene: Effects on fat and lean body mass in young and elderly women. Eur J Endocrinol 158:661-668. (Pubitemid 351639603)
26. McGuigan FE, Larzenius E, Callreus M, Gerdhem P, Luthman H, Akesson K. 2007. Variation in the BMP2 gene: Bone mineral density and ultrasound in young adult and elderly women. Calcif Tissue Int 81:254-262. (Pubitemid 47498100)
27. Mundy G, Garrett R, Harris S, Chan J, Chen D, Rossini G, Boyce B, Zhao M, Gutierrez G. 1999. Stimulation of bone formation in vitro and in rodents by statins. Science 286:1946-1949. (Pubitemid 129515901)
28. Natalizio BJ, Muniz LC, Arhin GK, Wilusz J, Lutz CS. 2002. Upstream elements present in the 3′-untranslated region of collagen genes influence the processing efficiency of overlapping polyadenylation signals. J Biol Chem 277:42733-42740. (Pubitemid 35285645)
29. Ogata T, Wozney JM, Benezra R, Noda M. 1993. Bone morphogenetic protein 2 transiently enhances expression of a gene, Id (inhibitor of differentiation), encoding a helix-loop-helix molecule in osteoblast-like cells. Proc Natl Acad Sci USA 90:9219-9222. (Pubitemid 23306484)
30. Plutzky J. 2007. A cardiologist's perspective on cardiometabolic risk. Am J Cardiol 100:3P-6P.
31. Reid IR. 2002. Relationships among body mass, its components, and bone. Bone 31:547-555. (Pubitemid 35449695)
32. Reneland RH, Mah S, Kammerer S, Hoyal CR, Marnellos G, Wilson SG, Sambrook PN, Spector TD, Nelson MR, Braun A. 2005. Association between a variation in the phosphodiesterase 4D gene and bone mineral density. BMC Med Genet 6:9. (Pubitemid 41418161)
33. Roelen BA, Dijke P. 2003. Controlling mesenchymal stem cell differentiation by TGFBeta family members. J Orthop Sci 8:740-748. (Pubitemid 37288325)
34. Rosen ED, MacDougald OA. 2006. Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7:885-896.
35. Rosen V, Thies R. 1992. The BMP proteins in bone formation and repair. Trends Genet 8:97-102.
36. Shao JS, Cai J, Towler DA. 2006. Molecular mechanisms of vascular calcification: Lessons learned from the aorta. Arterioscler Thromb Vasc Biol 26:1423-1430. (Pubitemid 44288965)
37. Shao JS, Cheng SL, Pingsterhaus JM, Charlton-Kachigian N, Loewy AP, Towler DA. 2005. Msx2 promotes cardiovascular calcification by activating paracrine Wnt signals. J Clin Invest 115:1210-1220. (Pubitemid 40629039)
38. Sottile V, Seuwen K. 2000. Bone morphogenetic protein-2 stimulates adipogenic differentiation of mesenchymal precursor cells in synergy with BRL 49653 (rosiglitazone). FEBS Lett 475:201-204. (Pubitemid 30408453)
39. Styrkarsdottir U, Cazier JB, Kong A, Rolfsson O, Larsen H, Bjarnadottir E, Johannsdottir VD, Sigurdardottir MS, Bagger Y, Christiansen C, Reynisdottir I, Grant SF, Jonasson K, Frigge ML, Gulcher JR, Sigurdsson G, Stefansson K. 2003. Linkage of osteoporosis to chromosome 20p12 and association to BMP2. PLoS Biol 1:E69. (Pubitemid 39112134)
40. Thompson PD, Moyna N, Seip R, Price T, Clarkson P, Angelopoulos T, Gordon P, Pescatello L, Visich P, Zoeller R, Devaney JM, Gordish H, Bilbie S, Hoffman EP. 2004. Functional polymorphisms associated with human muscle size and strength. Med Sci Sports Exerc 36:1132-1139. (Pubitemid 38878986)
41. Tosi LL, Boyan BD, Boskey AL. 2005. Does sex matter in musculoskeletal health? The influence of sex and gender on musculoskeletal health. J Bone Joint Surg Am 87:1631-1647. (Pubitemid 40917768)
42. Tracy BL, Ivey FM, Jeffrey Metter E, Fleg JL, Siegel EL, Hurley BF. 2003. A more efficient magnetic resonance imaging-based strategy for measuring quadriceps muscle volume. Med Sci Sports Exerc 35:425-433.
43. Tranah GJ, Taylor BC, Lui LY, Zmuda JM, Cauley JA, Ensrud KE, Hillier TA, Hochberg MC, Li J, Rhees BK, Erlich HA, Sternlicht MD, Peltz G, Cummings SR. 2008. Genetic variation in candidate osteoporosis genes, bone mineral density, and fracture risk: The study of osteoporotic fractures. Calcif Tissue Int 83:155-166.
44. Wang EA, Israel DI, Kelly S, Luxenberg DP. 1993. Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells. Growth Factors 9:57-71.
45. Wilusz CJ, Wilusz J. 2004. Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet 20:491-497. (Pubitemid 39201069)
46. Wilusz CJ, Wilusz J. 2007. HuR-SIRT: The hairy world of posttranscriptional control. Mol Cell 25:485-487. (Pubitemid 46274450)
47. Wilusz CJ, Wormington M, Peltz SW. 2001. The cap-to-tail guide to mRNA turnover. Nat Rev Mol Cell Biol 2:237-246.
48. Wilusz J, Shenk T. 1988. A 64 kd nuclear protein binds to RNA segments that include the AAUAAA polyadenylation motif. Cell 52:221-228. (Pubitemid 18042858)
49. Xiao YT, Xiang LX, Shao JZ. 2007. Bone morphogenetic protein. Biochem Biophys Res Commun 362:550-553.
50. Xiong DH, Shen H, Zhao LJ, Xiao P, Yang TL, Guo Y, Wang W, Guo YF, Liu YJ, Recker RR, Deng HW. 2006. Robust and comprehensive analysis of 20 osteoporosis candidate genes by very high-density single-nucleotide polymorphism screen among 405 white nuclear families identified significant association and gene-gene interaction. J Bone Miner Res 21:1678-1695. (Pubitemid 46141223)
51. Xu J, Rogers MB. 2007. Modulation of bone morphogenetic protein (BMP) 2 gene expression by Sp1 transcription factors. Gene 392:221-229. (Pubitemid 46486691)
52. Zhao J, Xiao P, Guo Y, Liu YJ, Pei YF, Yang TL, Pan F, Chen Y, Shen H, Zhao LJ, Papasian CJ, Drees BM, Hamilton JJ, Deng HY, Recker RR, Deng HW. 2008. Bivariate genome linkage analysis suggests pleiotropic effects on chromosomes 20p and 3p for body fat mass and lean mass. Genet Res 90:259-268. (Pubitemid 351973863)
53. Zhou S, Turgeman G, Harris SE, Leitman DC, Komm BS, Bodine PV, Gazit D. 2003. Estrogens activate bone morphogenetic protein-2 gene transcription in mouse mesenchymal stem cells. Mol Endocrinol 17:56-66. (Pubitemid 36132659)